Foyt began racing midgets in 1953 at age 18 in a car owned and maintained by his father. He started his USAC career in a midget car at the 1956 Night before the 500 in Anderson, Indiana. His first midget car win was at a 100 lap event at Kansas City in 1957, and finished seventh in the season points standings.[1] He left midget cars after the 1957 season to drive in sprint cars and Championship Car. He did occasionally compete in midget car events. He won the 1960 and 1961 Turkey Night Grand Prix, the first two years that it was held at Ascot Park. He won the 1961 Hut Hundred after starting last, and finished seventh in National Midget points that year. He won the 1970 Astro Grand Prix, an event that he promoted in his hometown of Houston. He ended his career with 20 midget car feature wins. Even after he had reached the pinnacle of his sport, Foyt was known to make occasional appearances in small, local events as a way of thanking promoters who had supported him in his struggle up the ladder.

Foyt began his sprint car career in 1956, at age 21, driving the Les Vaughn Offy with the International Motor Contest Association. On August 24, 1956, Foyt outqualified a field of 42 drivers at the Minnesota State Fair and, the following day, he won his first sprint car race, running away with the IMCA feature at the Red River Fair in Fargo, N.D. On June 16, 1957, on the high banked asphalt track at Salem, Indiana, Foyt came out on top in a race long battle with Bob Cleberg. That victory put Foyt on the radar for USAC car owners and he switched from the IMCA to USAC later that season. Foyt eventually won 28 USAC National sprint car feature races and the USAC Eastern Championship in 1960. Foyt continued to race sprint cars long after he was firmly established as one of the top drivers at the Indy 500.

In 1961, he became the first driver to successfully defend his points championship and win the Indianapolis 500 race. Late in the 500, Foyt made a pit stop for fuel, but a refueling malfunction meant that he returned to the race without enough fuel to finish. Eddie Sachs, unaware that Foyt's now-quicker car was light on fuel, pushed hard to keep up—and Sachs had to pit from the lead with just three laps remaining to replace a shredded right rear tire. Foyt pitted again also but only for enough fuel to finish. He took over the lead and beat Sachs by just 8.28 seconds—the second-closest finish in history at the time. He raced in each season from 1957–1992, starting in 374 races and finishing in the top ten 201 times, with 67 victories. In 1958, Foyt raced in Italy in the Trophy of the Two Worlds on the banking at Monza.

Ford-powered entries were widely expected to dominate the 1964 Indianapolis 500. Discussions between Ford officials and Foyt (who had a stock car contract with Ford at the time) took place early in the month of May about the possibility of Foyt taking over the third Team Lotus-Ford, a team reserve vehicle. Foyt wanted the use of the car for the entire month, but Lotus team owner Colin Chapman was reluctant to promise him the reserve car, in case something happened to cars driven by team drivers Jim Clark and Dan Gurney.

So discussions ended and Foyt stayed with his reliable, well-sorted Offenhauser-engined roadster. In the 1964 season, Foyt won a record 10 of 14 races en route to his championship, including the Indy 500. When the two fastest Lotus-Fords, driven by Jim Clark and Bobby Marshman, fell out of the race with mechanical problems, and Parnelli Jones was knocked out when his fuel tank exploded during a pit stop, Foyt was left alone at the front of the field, and cruised home to win his second Indianapolis 500. The race is remembered for the fiery second-lap crash that claimed the lives of Dave MacDonald and Eddie Sachs. Foyt did not learn of the fate of his two friends until he reached victory lane, and was handed a newspaper with a headline announcing the tragedy.

In August 1965, at the Milwaukee 200-mile (320 km) Championship Car race, Foyt's rear-engined Lotus pavement car was not at the track. So Foyt unloaded the Offenhauser-engined dirt track car he had won the 100-mile (160 km) race with at Springfield the previous day. He sprayed the mud off the car, installed pavement tires and a set-up for the one mile (1.6 km) oval. Foyt received permission to take two extra warm up laps during qualifying, as he had no time for practice. He then qualified the car on the pole, led the race for 18 out of 200 laps but then had to stop for a new rear tire, and finished second to Gordon Johncock, driving a rear-engined Gerhardt-Offy Indy car.

In the 1967 Indianapolis 500, Parnelli Jones' STP-Paxton Turbocar was expected to easily defeat the field of piston engines. Jones lapped the field, but his car expired with three laps remaining, and Foyt inherited the lead. As Foyt moved through turn three on the 200th lap, he slowed down. A few hundred yards ahead of him, Carl Williams spun out as he exited turn four, triggering a five-car front-stretch accident right in front of Foyt. Traveling at no more than 100 mph, Foyt threaded his way through the wreckage and safely took the checkered flag. The race took two days to complete when rain stopped the race on the 18th lap on the first day.

In the 1977 Indianapolis 500, Foyt ran out of fuel, and had to make a pit stop. He had to make up around 32 seconds on Gordon Johncock. Foyt made up 1.5 to 2 seconds per lap by turning up his turbo boost, which risked destroying the engine. Johncock's own engine expired just as Foyt had closed to within eight seconds back after both drivers' final pit stops, and Foyt passed for the win.

In 1981, Foyt was involved in an accident at the Michigan 500 and nearly lost an arm. It took him a while to get back to full fitness; and at the Indy 500 the following year he qualified third.

Foyt won the Indianapolis 500 four times, in 1961, 1964, 1967 and 1977. He is the first driver to have done so. The feat has since been matched by Al Unser (1970, 1971, 1978, 1987) and Rick Mears (1979, 1984, 1988, 1991). Of his 67 career Championship Car race victories, twelve were won at Trenton Speedway. Foyt also won the Indycar Series seven times, a record that still stands.

Foyt's worst Indy 500 finish is 31st in the 1982 event. Foyt started on the front row but on the pace laps he was victimized by a controversial wreck when rookie Kevin Cogan suddenly spun out for no apparent reason. Cogan wrecked seven cars in the incident including Foyt and Mario Andretti. Foyt was livid with Cogan and famously said "That damn Coogan," on live radio, and when asked by Chris Economaki who wrecked him in an interview, Foyt shouted "Coogan". Foyt repaired his car during the red flag, and led the first quarter of the race but dropped out due to damages linked to the Cogan crash.

Foyt is famous for winning the prestigious 24 Hours of Le Mans race in his first and only attempt, in 1967; Foyt drove a Ford GT40 Mk IV, partnered with Dan Gurney and entered by Carroll Shelby's team. Prior to the race, he had angered the French fans and press by remarking that the notoriously fast and dangerous tree-lined course was "nothin' but a little old country road."[5] Also, he reportedly only got 10 laps of pre-race practice. But when Gurney overslept and missed a driver change in the middle of the night, Foyt was forced to double-stint and wound up driving nearly 18 hours of the 24-hour race. While being sprayed with champagne on the victory podium, he is reported to have asked, "Do I win rookie of the year?" Foyt also later won the 12 Hours of Sebring and 24 Hours of Daytona during the 1980s driving Porsches, making him one of only 12 drivers to complete the "triple crown" of endurance racing.

Foyt, a veteran who had been racing professionally for eight seasons before trying his hand at NASCAR racing, only needed ten races to get his first victory. Richard Petty dominated the 1964 Firecracker 400 until he dropped out with engine problems. Foyt swapped the lead with Bobby Isaac for the final 50 laps of the summer event at the Daytona International Speedway. Foyt passed Isaac on the final lap to win the race.

In January 1965, Foyt qualified and ran in the front of the pack most of the day with Dan Gurney and Parnelli Jones in the Motor Trend 500 at Riverside. Parnelli retired with mechanical issues, leaving Gurney and Foyt to contest the lead. Late in the race, dueling with Gurney, Foyt spun. His car refired, and he charged through the field in an attempt to regain lost positions. After running hard to catch leader Gurney, Foyt's brakes failed entering turn nine at the end of Riverside's mile-long, downhill back straight. Foyt turned the car into the infield at more than 100 mph, and the car tumbled violently end-over-end several times. The track doctor at Riverside International Raceway pronounced Foyt dead at the scene of the severe crash, but fellow driver Parnelli Jones revived him after seeing movement. Foyt suffered severe chest injuries, a broken back, and a fractured ankle. Footage of his flipping No. 00 Ford, owned by Holman Moody, is featured in the final scene of the movie Redline 7000.

Foyt ran out of gas near the end of the 1971 Daytona 500, and Petty passed him for the win. Foyt again had the car to beat in the 1972 Daytona 500, but this time succeeded in a dominant performance. Only three drivers led during the race. In 1979 at the Daytona 500, Foyt was running in fifth place, but when Cale Yarborough and Donnie Allison had their famous tangle on the final lap, Foyt finished in third spot behind Darrell Waltrip and Richard Petty who again won the race. When Foyt pulled up next to Petty after the checkers to congratulate him, he was called "a true gentleman" during the broadcast.

In 1988 Foyt was banned from NASCAR for six months and fined $20,000 following a series of incidents during the Winston 500. His ban was reduced to two months following an appeal and his fine was raised to $35,000.

Foyt's final NASCAR Winston Cup Series race was the 1994 Brickyard 400, the inaugural running of that race. Foyt finished 30th, four laps behind winner Jeff Gordon. Foyt entered the race again in 1995 and 1996, but failed to qualify both times. In 1995, his attempt was stymied when rain washed out second round time trials.

Foyt ended up racing three times in the early days of the NASCAR Craftsman (now Camping World) Truck Series, with a best finish of 18th coming in the 1995 GM Goodwrench / Delco Battery 200, a race for which he qualified ninth.

Foyt and Mario Andretti are the only men to have won both the Indianapolis and Daytona 500s.

Foyt holds the closed course speed record driving the Oldsmobile Aerotech at an average speed of 257.123 miles per hour (413.799 km/h). He set the record on 27 August 1987 at a 7.712-mile (12.411 km) test track near Fort Stockton, Texas.

Despite having won more USAC sanctioned events than any other driver Foyt never won a CART sanctioned event.

Foyt has numerous career records at the Indianapolis 500: the first of to date three drivers to have won a record four times, the most consecutive and career starts (35), most races led (13), most times led during the career (39), and most competitive laps and miles during a career (4,909 laps, 12,272.5 miles). In the 1961 Indianapolis 500 Foyt won over Eddie Sachs with a lead of 8.28 seconds, the second closest finish in Indianapolis history at the time. Shortly thereafter, Foyt and Ray Harroun (who won the first Indianapolis 500 in 1911) appeared together on a segment of the TV program I've Got a Secret—their secret being their respective wins 50 years apart.

As of November 2011, Foyt stands as only the third-oldest living winner of the Indianapolis 500 (Parnelli Jones and Bobby Unser are older), but the longest-ago living winner (1961).

Scott Sharp took a share of the 1996 Indy Racing League (IRL) title driving for Foyt while Kenny Bräck won the 1998 IRL title, also in a Foyt car. Bräck won the 1999 Indianapolis 500 in Foyt's car, putting Foyt in the winner's circle at Indy for the fifth time. The current driver for his IRL team, A. J. Foyt Enterprises, is Takuma Sato. On June 7, 1997, Foyt (as an owner) was involved in an incident that helped shape the history of the Indy Racing League and added to his reputation as a man of little patience. One of his drivers, Billy Boat, had been declared the winner of the inaugural IRL race at Texas Motor Speedway that had been held that night, and his other driver, Davey Hamilton, had come in second. However, Dutch driver Arie Luyendyk disputed Boat's win, claiming that he was in the lead when a scoring error by USAC (who had scored all IRL races up until that time) gave Boat the checkered flag. When Luyendyk entered victory lane after the race to confront TMS general manager Eddie Gossage about the finish uttering obscenities, an irate Foyt approached Luyendyk from behind and slapped and shoved him into a tulip bed (ironically given Luyendyk's Dutch nationality). Luyendyk then requested a review of the race; a few days later, USAC reversed its position and declared Luyendyk the winner; Foyt kept the victory lane-awarded trophy. Following the controversy, the IRL relieved USAC of the scoring duties for its events.

Foyt is the grandfather of A. J. Foyt IV. Foyt is the grandfather and adoptive father of Larry Foyt. He is also the godfather of driver John Andretti. When not busy with the racing season, A.J. Foyt likes to spend time at the family Ranches, The Foyt Ranch located in Hockley, Texas and Brackettville, Texas.

The Foyts are also, via marriage, part of the ownership group of the Indianapolis Colts. A. J. Foyt IV is married to the daughter of Colts owner Jim Irsay.